Effect of Signal Peptide on Stability and Folding of Escherichia coli Thioredoxin

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Singh, Pranveer ^a,c   Sharma, Likhesh ^a   Kulothungan, S Rajendra ^a   Adkar, Bharat V ^a   Prajapati, Ravindra Singh ^a   Ali, P Shaik Syed ^a   Krishnan, Beena ^a   Varadarajan, Raghavan ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^c INDIRA GANDHI NATIONAL TRIBAL UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; HYBRID PROTEIN; MALE THIOREDOXIN FUSION PROTEIN; PELB THIOREDOXIN FUSION PROTEIN; SIGNAL PEPTIDE; THIOREDOXIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; COMPARATIVE STUDY; CONTROLLED STUDY; ESCHERICHIA COLI; IN VITRO STUDY; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN REFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; THERMOSTABILITY; WILD TYPE;

AMINO ACID SEQUENCE; ANILINO NAPHTHALENESULFONATES; BUFFERS; CALORIMETRY, DIFFERENTIAL SCANNING; CHROMATOGRAPHY, GEL; CIRCULAR DICHROISM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GUANIDINE; INSULIN; MOLECULAR SEQUENCE DATA; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN SORTING SIGNALS; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; THIOREDOXINS;

EID: 84877156114     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063442     Document Type: Article

References (61)

1. Pugsley AP, (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57: 50-108.
2. Stuart RA, Neupert W (2000) Making membranes in bacteria. Nature 406: 575, 577.
3. Cristobal S, de Gier JW, Nielsen H, von Heijne G, (1999) Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J 18: 2982-2990.
4. DeLisa MP, Tullman D, Georgiou G, (2003) Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci U S A 100: 6115-6120.
5. Izard JW, Kendall DA, (1994) Signal peptides: exquisitely designed transport promoters. Mol Microbiol 13: 765-773.
6. du Plessis DJ, Nouwen N, Driessen AJ, (2011) The Sec translocase. Biochim Biophys Acta 1808: 851-865.
7. Hartl FU, Lecker S, Schiebel E, Hendrick JP, Wickner W, (1990) The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 63: 269-279.
8. Hoffschulte HK, Drees B, Muller M, (1994) Identification of a soluble SecA/SecB complex by means of a subfractionated cell-free export system. J Biol Chem 269: 12833-12839.
9. Randall LL, Hardy SJ, (1986) Correlation of competence for export with lack of tertiary structure of the mature species: a study in vivo of maltose-binding protein in E. coli. Cell 46: 921-928.
10. Kusukawa N, Yura T, Ueguchi C, Akiyama Y, Ito K, (1989) Effects of mutations in heat-shock genes groES and groEL on protein export in Escherichia coli. EMBO J 8: 3517-3521.
11. Wild J, Altman E, Yura T, Gross CA, (1992) DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev 6: 1165-1172.
12. Randall LL, Hardy SJ, (1995) High selectivity with low specificity: how SecB has solved the paradox of chaperone binding. Trends Biochem Sci 20: 65-69.
13. Francetic O, Kumamoto CA, (1996) Escherichia coli SecB stimulates export without maintaining export competence of ribose-binding protein signal sequence mutants. J Bacteriol 178: 5954-5959.
14. Krishnan B, Kulothungan SR, Patra AK, Udgaonkar JB, Varadarajan R, (2009) SecB-mediated protein export need not occur via kinetic partitioning. J Mol Biol 385: 1243-1256.
15. Kulothungan SR, Das M, Johnson M, Ganesh C, Varadarajan R, (2009) Effect of crowding agents, signal peptide, and chaperone SecB on the folding and aggregation of E. coli maltose binding protein. Langmuir 25: 6637-6648.
16. Zalucki YM, Jones CE, Ng PS, Schulz BL, Jennings MP, (2010) Signal sequence non-optimal codons are required for the correct folding of mature maltose binding protein. Biochim Biophys Acta 1798: 1244-1249.
17. Zalucki YM, Shafer WM, Jennings MP, (2011) Directed evolution of efficient secretion in the SRP-dependent export of TolB. Biochim Biophys Acta 1808: 2544-2550.
18. Robbens J, Raeymaekers A, Steidler L, Fiers W, Remaut E, (1995) Production of soluble and active recombinant murine interleukin-2 in Escherichia coli: high level expression, Kil-induced release, and purification. Protein Expr Purif 6: 481-486.
19. Wan EW, Baneyx F, (1998) TolAIII co-overexpression facilitates the recovery of periplasmic recombinant proteins into the growth medium of Escherichia coli. Protein Expr Purif 14: 13-22.
20. Schatz PJ, Beckwith J, (1990) Genetic analysis of protein export in Escherichia coli. Annu Rev Genet 24: 215-248.
21. Walter P, Johnson AE, (1994) Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu Rev Cell Biol 10: 87-119.
22. von Heijne G, (1985) Signal sequences. The limits of variation. J Mol Biol 184: 99-105.
23. Sjostrom M, Wold S, Wieslander A, Rilfors L, (1987) Signal peptide amino acid sequences in Escherichia coli contain information related to final protein localization. A multivariate data analysis. EMBO J 6: 823-831.
24. Edman M, Jarhede T, Sjostrom M, Wieslander A, (1999) Different sequence patterns in signal peptides from mycoplasmas, other gram-positive bacteria, and Escherichia coli: a multivariate data analysis. Proteins 35: 195-205.
25. Humphreys DP, Sehdev M, Chapman AP, Ganesh R, Smith BJ, et al. (2000) High-level periplasmic expression in Escherichia coli using a eukaryotic signal peptide: importance of codon usage at the 5′ end of the coding sequence. Protein Expr Purif 20: 252-264.
26. Lei SP, Lin HC, Wang SS, Callaway J, Wilcox G, (1987) Characterization of the Erwinia carotovora pelB gene and its product pectate lyase. J Bacteriol 169: 4379-4383.
27. Steiner D, Forrer P, Stumpp MT, Pluckthun A, (2006) Signal sequences directing cotranslational translocation expand the range of proteins amenable to phage display. Nat Biotechnol 24: 823-831.
28. Josefsson LG, Randall LL, (1983) Analysis of cotranslational proteolytic processing of nascent chains using two-dimensional gel electrophoresis. Methods Enzymol 97: 77-85.
29. Schierle CF, Berkmen M, Huber D, Kumamoto C, Boyd D, et al. (2003) The DsbA signal sequence directs efficient, cotranslational export of passenger proteins to the Escherichia coli periplasm via the signal recognition particle pathway. J Bacteriol 185: 5706-5713.
30. Holmgren A, (1968) Thioredoxin. 6. The amino acid sequence of the protein from escherichia coli B. Eur J Biochem 6: 475-484.
31. Eklund H, Gleason FK, Holmgren A, (1991) Structural and functional relations among thioredoxins of different species. Proteins 11: 13-28.
32. Katti SK, LeMaster DM, Eklund H, (1990) Crystal structure of thioredoxin from Escherichia coli at 1.68 A resolution. J Mol Biol 212: 167-184.
33. Jeng MF, Campbell AP, Begley T, Holmgren A, Case DA, et al. (1994) High-resolution solution structures of oxidized and reduced Escherichia coli thioredoxin. Structure 2: 853-868.
34. Slaby I, Cerna V, Jeng MF, Dyson HJ, Holmgren A, (1996) Replacement of Trp28 in Escherichia coli thioredoxin by site-directed mutagenesis affects thermodynamic stability but not function. J Biol Chem 271: 3091-3096.
35. Holmgren A, (1972) Tryptophan fluorescence study of conformational transitions of the oxidized and reduced form of thioredoxin. J Biol Chem 247: 1992-1998.
36. Kelley RF, Stellwagen E, (1984) Conformational transitions of thioredoxin in guanidine hydrochloride. Biochemistry 23: 5095-5102.
37. Kelley RF, Shalongo W, Jagannadham MV, Stellwagen E, (1987) Equilibrium and kinetic measurements of the conformational transition of reduced thioredoxin. Biochemistry 26: 1406-1411.
38. Pedone E, Bartolucci S, Rossi M, Pierfederici FM, Scire A, et al. (2003) Structural and thermal stability analysis of Escherichia coli and Alicyclobacillus acidocaldarius thioredoxin revealed a molten globule-like state in thermal denaturation pathway of the proteins: an infrared spectroscopic study. Biochem J 373: 875-883.
39. Nielsen H, Engelbrecht J, Brunak S, von Heijne G, (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
40. Ghoshal AK, Swaminathan CP, Thomas CJ, Surolia A, Varadarajan R, (1999) Thermodynamic and kinetic analysis of the Escherichia coli thioredoxin-C′ fragment complementation system. Biochem J 339 (Pt 3): 721-727.
41. Ganesh C, Shah AN, Swaminathan CP, Surolia A, Varadarajan R, (1997) Thermodynamic characterization of the reversible, two-state unfolding of maltose binding protein, a large two-domain protein. Biochemistry 36: 5020-5028.
42. Sheshadri S, Lingaraju GM, Varadarajan R, (1999) Denaturant mediated unfolding of both native and molten globule states of maltose binding protein are accompanied by large deltaCp's. Protein Sci 8: 1689-1695.
43. Agashe VR, Udgaonkar JB, (1995) Thermodynamics of denaturation of barstar: evidence for cold denaturation and evaluation of the interaction with guanidine hydrochloride. Biochemistry 34: 3286-3299.
44. Holmgren A, (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem 254: 9627-9632.
45. Tartaglia GG, Vendruscolo M, (2008) The Zyggregator method for predicting protein aggregation propensities. Chem Soc Rev 37: 1395-1401.
46. Trovato A, Seno F, Tosatto SC, (2007) The PASTA server for protein aggregation prediction. Protein Eng Des Sel 20: 521-523.
47. Conchillo-Sole O, de Groot NS, Aviles FX, Vendrell J, Daura X, et al. (2007) AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8: 65.
48. Varadarajan R, Nagarajaram HA, Ramakrishnan C, (1996) A procedure for the prediction of temperature-sensitive mutants of a globular protein based solely on the amino acid sequence. Proc Natl Acad Sci U S A 93: 13908-13913.
49. Beena K, Udgaonkar JB, Varadarajan R, (2004) Effect of signal peptide on the stability and folding kinetics of maltose binding protein. Biochemistry 43: 3608-3619.
50. Chakraborty K, Thakurela S, Prajapati RS, Indu S, Ali PS, et al. (2005) Protein stabilization by introduction of cross-strand disulfides. Biochemistry 44: 14638-14646.
51. Woody RW, (1995) Circular dichroism. Methods Enzymol 246: 34-71.
52. Chakrabarti A, Srivastava S, Swaminathan CP, Surolia A, Varadarajan R, (1999) Thermodynamics of replacing an alpha-helical Pro residue in the P40S mutant of Escherichia coli thioredoxin. Protein Sci 8: 2455-2459.
53. Das M, Kobayashi M, Yamada Y, Sreeramulu S, Ramakrishnan C, et al. (2007) Design of disulfide-linked thioredoxin dimers and multimers through analysis of crystal contacts. J Mol Biol 372: 1278-1292.
54. Zimmerman SB, Minton AP, (1993) Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct 22: 27-65.
55. Debarbieux L, Beckwith J, (1998) The reductive enzyme thioredoxin 1 acts as an oxidant when it is exported to the Escherichia coli periplasm. Proc Natl Acad Sci U S A 95: 10751-10756.
56. Huber D, Boyd D, Xia Y, Olma MH, Gerstein M, et al. (2005) Use of thioredoxin as a reporter to identify a subset of Escherichia coli signal sequences that promote signal recognition particle-dependent translocation. J Bacteriol 187: 2983-2991.
57. Milstein C, Brownlee GG, Harrison TM, Mathews MB, (1972) A possible precursor of immunoglobulin light chains. Nat New Biol 239: 117-120.
58. Blobel G, Dobberstein B, (1975) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67: 835-851.
59. Fekkes P, Driessen AJ, (1999) Protein targeting to the bacterial cytoplasmic membrane. Microbiol Mol Biol Rev 63: 161-173.
60. Hardy SJ, Randall LL, (1991) A kinetic partitioning model of selective binding of nonnative proteins by the bacterial chaperone SecB. Science 251: 439-443.
61. Huber D, Cha MI, Debarbieux L, Planson AG, Cruz N, et al. (2005) A selection for mutants that interfere with folding of Escherichia coli thioredoxin-1 in vivo. Proc Natl Acad Sci U S A 102: 18872-18877.